Testis size depends on social status and the presence of male helpers in the cooperatively breeding cichlid Julidochromis ornatus

Cooperatively breeding animals, in which helpers may participatein reproduction with dominant breeders, are ideal species forexamining intraspecific variation in testis size because theyoften exhibit both monogamous breeding (low risk of sperm competition)and polyandrous breeding (high risk) within a population. However,little is known about testis investment as a result of spermcompetition in these animals. The substrate-brooding cichlidfish Julidochromis ornatus has a cooperatively breeding system,in which some males mate monogamously and other males reproduceas dominant breeders or helpers within cooperatively breedinggroups, in which male helpers frequently sire young. We examinedthe relationship between testis investment and male social statusin relation to the risk of sperm competition. As predicted fromsperm competition models, in groups with male helpers, boththe male breeders and the male helpers invested more in testesmass, compared to breeding males without male helpers. We alsofound a positive relationship between the testes mass of malebreeders and their male helpers, suggesting that males increasetheir investment in reproductive capability under the risk ofsperm competition. Sperm competition models also predict thatlarger testes are associated with increased siring success.Our paternity analysis supported this prediction; we found apositive relationship between testis investment by male helpersand the number of offspring they sired.     

Is there an optimal number of helpers in Alpine marmot family groups?

The consequence of helping behavior on breeders fitness is stillcontroversial. We used multivariate analyses to investigatefor the effects of male and female subordinates on breeders'components of fitness in the Alpine marmot, Marmota marmota.We found that male and female subordinates, respectively, increasedand decreased juvenile survival during winter. Thus, we giveevidence that male subordinates should be considered as helpers,and that helpers provided breeders with immediate reproductivesuccess gains, whereas subordinates females were costly. Helpershad no positive effects on female body condition, on persistence(future survival) of dominants, and on future reproduction (occurrenceand size of a litter). Helpers thus did not provide breederswith delayed fitness benefits, and therfore, the load-lighteninghypothesis was not supported. On the contrary, helpers had delayedfitness cost for dominant males and, consequently, for dominantfemales. Immediate benefits counterbalanced by delayed costssuggested an optimal number of helpers in the family group bothfrom male and female perspectives. An optimality model wellpredicted the observed mean number of helpers in Alpine marmotfamily groups. Optimal numbers of helpers were slightly differentfor males and females, suggesting a potential conflict of interestbetween dominants. We finally discuss the possible mechanismsof helping that may explain the observed pattern in the Alpinemarmot.     

Cichlids do not adjust reproductive skew to the availability of independent breeding options

Helpers in cooperatively breeding species forego all or partof their reproduction when remaining at home and assisting breedersto raise offspring. Different models of reproductive skew generatealternative predictions about the share of reproduction unrelatedsubordinates will get depending on the degree of ecologicalconstraints. Concession models predict a larger share when independentbreeding options are good, whereas restraint and tug-of-warmodels predict no effects on reproductive skew. We tested thesepredictions by determining the share of reproduction by unrelatedmale and female helpers in the Lake Tanganyika cichlid Neolamprologuspulcher depending on experimentally manipulated possibilitiesfor helper dispersal and independent breeding and dependingon helper size and sex. We created 32 breeding groups in thelaboratory, consisting of two breeders and two helpers each,where only the helpers had access to a nearby dispersal compartmentwith (treatment) or without (control) breeding substrate, usinga repeated measures design. We determined the paternity andmaternity of 1185 offspring from 47 broods using five to nineDNA microsatellite loci and found that: (1) helpers participatedin reproduction equally across the treatments, (2) large malehelpers were significantly more likely to reproduce than smallhelpers, and (3) male helpers engaged in significantly morereproduction than female helpers. Interestingly, in four broods,extragroup helper males had fertilized part of the brood. Nohelper evictions from the group after helper reproduction wereobserved. Our results suggest that tug-of-war models based oncompetition over reproduction within groups describe best thereproductive skew observed in our study system. Female breedersproduced larger clutches in the treatment compared to the controlsituation when the large helpers were males. This suggests thatmale breeder-male helper reproductive conflicts may be alleviatedby females producing larger clutches with helpers around.     

Fitness consequences of helping behavior in the western bluebird

We examined the fitness consequences of helping behavior inthe western bluebird (Sialia mexicana) at Hastings Reservationin Carmel Valley, California, USA, and tested hypotheses forhow helpers benefit from engaging in alloparental behavior.Both juvenile and adult western bluebirds occasionally helpat the nest During a 12 year period, all adult helpers and mostjuvenile helpers were male. Helpers usually fed at nests ofboth their parents and rarely helped when only one parent waspresent. The frequency of pairs with adult helpers was only7%, but nearly one-third of adult males helped among those withboth parents on the study area. At least 28% were breeders whosenests failed. The propensity to help appears to depend uponparental survival, male philopatry, and the breeding successof potential helpers. Feeding rates were not increased at nestswith juvenile helpers, apparendy because breeding males reducedtheir feeding rates. In contrast, adult helpers increased theoverall rates of food delivery to the nest in spite of a reductionin the number of feeding trips made by both male and femaleparents. Helpers did not derive any obvious direct fitness benefitsfrom helping, but they had greater indirect fitness than nonhelpersdue to increases in nestling growth rates and fledging successat their parents' nests. Helpers fledged fewer offspring intheir first nests than did nonhelpers, suggesting that theywere birds with reduced reproductive potential. Although wehave not yet measured the effect of extrapair fertilizationson the fitness benefits of helping, we calculated the differencein fitness between helpers and nonhelpers as a function of thepotential helper's paternity when breeding independently andhis father's paternity in the nest at which he might help. Inconjunction with constraints on breeding and indirect fitnessbenefits, we predict that relatedness of males to the youngin their own as well as their parents' nests will influencehelping behavior in western bluebirds.     

Reproductive parasitism of broodcare helpers in a cooperatively breeding fish

Large male helpers in the cooperatively breeding cichlid Neolamprologus pulchergain reproductive success by parasitizing the reproductive effort ofmale territory owners. Under controlled, experimental conditionswe examined the genetic relatedness between the members of broodpairs (n = 14), their male helpers (n = 8), and offspring (n= 292) in seven families. We used multilocus DNA fingerprintingto check for potential reproductive parasitism by male helpersand to assess their fertilization success. Of offspring producedin these families, 10.3% were sired by helpers. In parasitizedbroods, helper fertilization success varied between 12.5% and35.8%. Male helpers parasitized parental reproduction when theirbody size exceeded 4.5 cm standard length (SL), even thoughsexual maturity may be reached much earlier (3.5 cm SL). Twoof three parasitic helpers were punished by severe aggressiveattacks when parasitizing the reproduction of breeders, whichled to their expulsion from the territory. This study demonstratesa potential fitness benefit to broodcare helpers that is oftenneglected. It also points to the delicate balance that may exist betweencooperative and competitive behavior in cooperatively breeding species.     

Family status and contributions to breeding by Florida scrub jays

Nestling care by Florida scrub jay Aphelocoma c. coerulescens breeders and helpers is quantified. Breeding males and older male helpers deliver more food than first-year helpers and older female helpers. Breeding males adjust the quantity of food they deliver inversely to that delivered by their helpers. Older female helpers, who make many nest visits without delivering food, attempt to usurp the nest-sitting role of the breeding female. The advantages of group breeding to the breeders seem clear. Pairs with helpers live longer and produce more fledglings. The advantages of being a helper, though obscure, probably include non-altruistic factors such as increased survival and, for males, increased chances of obtaining space for breeding. Food contributions of helpers seem to parallel these opportunities.     

Avian Helpers at the Nest: Are they Psychologically Castrated?

In cooperatively breeding pied kingfishers (Ceryle rudis) blood plasma levels of LH and testosterone (T) were compared among three types of males: breeders, primary (= related) helpers and secondary (= unrelated) helpers. These categories did not differ in LH, but primary helpers had significantly lower T titers than breeders and secondary helpers. The low levels were paralleled by small gonad sizes and no sperm production, suggesting that primary helpers were not able to fertilize eggs. The differences in T levels could neither be attributed to stochastic variation nor to differences in age, stress, molt, or reproductive activities. The most likely explanation arises from the observation that primary helpers are behaviorally dominated by breeders, whereas secondary helpers are not. The adaptive significance of low T titers and reduced fertility as a result from being dominated is discussed on the basis of empirical data and theoretical models. We argue that primary helpers in the pied kingfisher, and subordinate helpers in many other cooperative breeders, apparently are not “unwillingly” suppressed in their sexual development; they rather “choose” delayed reproduction when the costs from sexual competition with breeders exceed the benefits from cooperative breeding. In contrast, helpers that benefit more from competition than from cooperation, as secondary helpers do, cannot be expected to show reduced fertility.     

Cooperative Breeding and Group Structure in the Lake Tanganyika Cichlid Neolamprologus savoryi

As yet, cooperative breeding has been described only for some fish species. However, evidence is accumulating that it is widespread among Lake Tanganyika cichlids. We studied the cooperative breeding system of the substrate breeding cichlid Neolamprologus savoryi. Breeding groups typically consisted of a large breeding male with one to four breeding females and three to 33 helpers (mean group size: 14.3 members). Group size was significantly related to breeding male and female body sizes, and larger males had more breeding females and larger sized male helpers. The size of the largest female in the group was positively related to the number and sizes of secondary breeding females and female helpers. In case of multiple breeding females, these females usually divided the group's territory into sub‐territories, each with its own helpers (subgroups). Interspersed between groups, independent fish were detected defending an individual shelter (4.4% of all fish). In 9% of the groups no breeding female was present. All group members participated in territory defence and maintenance, and showed submissive behaviours to larger group members. As expected, the level of between‐subgroup conflicts was high compared with the level of within‐subgroup conflicts. We compare these results with data available from other cooperatively breeding fishes.     

Parasitic spawning in sand gobies: an experimental assessment of nest-opening size, sneaker male cues, paternity, and filial cannibalism

Sneaking is common in nest-building fish with paternal care,but the role of nest-opening size in protecting against entryby sneaker males has never been tested before. Using the sandgoby (Pomatoschistus minutus), a fish with exclusive paternalcare, experimental manipulations of nest openings provided nosupport for the hypothesis that nest openings serve as physicalor visual defense or that sneaker males prefer to parasitizenests with wide openings. Female mating preference was alsonot influenced by nest-opening size. However, female courtshipbehavior and visibility were important cues for sneaker males.Most sneak entries occurred when the nest holder was occupiedwith courtship, chasing another sneaker male or nest building.In half the cases of observed sneak entry, the sneaker malefertilized eggs, also when sneaking only occurred before spawning.Sneak entry and its duration were good estimates of stolen paternity,but neither sneak entries nor degree of fertilizations werecorrelated with filial cannibalistic behavior. Testes size didnot explain parasitic spawning success in replicates with geneticallydetermined sneaking. However, all sneaker males without breedingcoloration had huge testes and small sperm duct glands, whereasnest-holding males had small testes and large sperm duct glands,and sneaker males with breeding coloration were intermediate.     

First field evidence for alloparental egg care in cooperatively breeding fish

Helping behaviour in cooperative breeders has been intensively studied in many animal taxa, including arthropods, birds and mammals. In these highly social systems, helpers typically engage in brood care and the protection of dependent young. Such helping systems also exist in cooperatively breeding cichlid species of Lake Tanganyika. However, breeding in these species happens in clefts, narrow holes or shelters underneath stones. Therefore, direct brood care by breeders and helpers has thus far only been observed under artificial laboratory conditions. Under natural conditions, brood care behaviour has been estimated indirectly by determining the time spent in the breeding chamber, or by the number of visits to the breeding chamber. The reliability of such substitutes needs to be validated, for instance, by demonstrating alloparental egg care of helpers through direct observations in nature. Here, we describe direct egg care by a male helper of the cooperatively breeding cichlid Neolamprologus savoryi in the field. The helper inspected and cleaned the eggs and defended them against predators. By reconstructing the genetic relatedness using microsatellite markers, we show that the helper was the son of the breeding male, but unrelated to the breeding female. The genetic mother of the helper was defending a different territory next to the one where the helper showed alloparental egg care. This indicates that the helper had dispersed inside the male territory to assist another female to care for his half‐siblings. These results demonstrate alloparental egg care without reproductive share in a fish species under natural conditions, underlining that helping behaviour in cooperatively breeding fish has a strong non‐self‐serving component.     

Male Seychelles warblers use territory budding to maximize lifetime fitness in a saturated environment

In cooperatively breeding species, helping at the nest and buddingoff part of the natal territory have been advanced as strategiesto increase fitness in an environment that is saturated withterritories. The importance of helping or territory buddingas a determinant of lifetime reproductive success (LRS) hasbeen debated because the potential benefits of both strategiescould not be separated. Here we test the causes and the immediateand future fitness consequences of single dispersal decisionstaken by male Seychelles warblers (Acrocephalus sechellensis).Males breeding in high-quality territories (high food abundance)have significantly higher LRS than similar-aged males buddingoff part of the parental territory. Initially, budders havea low reproductive success (because of limited food resourcesor absence of a breeding partner). However, they have a longlife span and inherit high-quality territories through sitedominance, by which they gain higher LRS than breeders on low-qualityterritories, helpers, or floaters. Experimental creation ofmale breeding territory vacancies showed that most young malesbecame budders because of intense competition for high-quality territories. The translocation of warblers to the previouslyunoccupied Aride Island shows that males behave according tothe expected fitness benefits of each dispersal strategy. Inthe absence of competition for territories on Aride, all youngmales bred in high-quality territories. However, after saturationof high-quality habitat with territories, most males becamebudders rather than breeders on low-quality habitat, helpers,or floaters.     

Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish

Several hypotheses aim to explain the evolution of helping behavior,but conclusive experimental support for evaluating the relativeimportance of individual hypotheses is still lacking. We reporton two field experiments conducted to test the "territory inheritance"and "pay-to-stay" hypotheses in the cooperatively breeding cichlidfish Neolamprologus pulcher The territory inheritance hypothesiswas tested by removing one parent, which created breeding vacancies.In 39% of cases, same-sex helpers took over the breeding spot;in 44% of cases helpers continued helping new breeders, and17% were evicted by new breeders. Helpers that were closelysize matched to the removed breeder had a better chance of gainingthe breeding spot Male helpers tended to continue helping aftera takeover more often than females.The pay-to-stay hypothesiswas tested-by temporarily removing helpers. Whereas breedersdid not respond aggressively to removals, other group membersattacked the removed helpers on their return, and 29% were eventuallyevicted. The returning helpers assisted more by increasing theirrate of territory maintenance and defense and visiting the broodchamber more frequently Size and sex of removed helpers didnot explain the observed aggressive reactions of other groupmembers. Thus, our results support both hypotheses: N. pulcherneeds to pay with help to be allowed to remain protected inthe family group, and there they may inherit the natal territory.N. pulcher helpers gain direct benefits from helping behavior.     

The role of prolactin in the regulation of brood care in the cooperatively breeding fish Neolamprologus pulcher

The hormone prolactin (PRL) is important for the regulation of parental care in many species of mammals, birds and fish, and for alloparental care (care directed at nondescendant young) in some mammals and birds. Its significance in alloparental brood care of cooperatively breeding fish has not yet been assessed. Here, we test the role of PRL in brood care behavior of the cooperatively breeding cichlid Neolamprologus pulcher. The expression of PRL mRNA was determined in the pituitary glands of breeders of both sexes, helpers that showed brood care behavior and nonbreeding fish as controls. In addition, PRL levels were experimentally manipulated in male breeders and helpers by intraperitoneal injections of ovine PRL, and the behavior of these test fish was recorded toward standardized clutches. Adult females had higher levels of PRL mRNA than adult males, which was true both for breeders and nonbreeders. Contrary to expectation, there was no positive correlation between PRL and brood care behavior in any category of test fish, and the experimental application of PRL did not change brood care propensity. Interestingly, brood-caring adult females had significantly lower levels of PRL mRNA than adult female nonbreeders, whereas there was no difference between helpers and similar-sized nonbreeding group members. PRL mRNA levels increased with body mass in juveniles, but decreased with body mass in adults. In conclusion, we found no evidence that elevated levels of PRL are directly involved in the regulation of brood care behavior in this species.     

Group Structure,Nest Size and Reproductive Success in the Cooperatively Breeding Cichlid Julidochromis ornatus: A Correlation Study

The effect of group size on reproductive success has long been studied in cooperatively breeding species, as it might provide an adaptive explanation for group‐living in social species. Numerous studies have shown positive effects of subordinates on reproductive success (‘helper effect’), but these studies have also revealed the importance of controlling statistically, or experimentally, for the effect of other factors that might affect reproductive success. Here, we first examine the relationships between group size, body size of group members and nest size in the cooperatively breeding cichlid Julidochromis ornatus, in which unrelated helpers frequently participate in reproduction and their breeding nests inside rock crevices may be crucial for reproduction and survival of all group members. Then, we subsequently investigate the relationship between group size and reproductive success, while controlling for these factors. The results showed that group size was significantly related to body size of group members rather than nest size; and larger breeders had larger helpers. It was found that group size significantly increased group reproductive output. More importantly, reproductive success of male breeders did not depend on the presence of mature helpers, whereas female reproductive success increased when two males assisted her and tended to decrease when two females bred cooperatively. We conclude that breeding groups of J. ornatus have size hierarchical societies that relate to group size, and group composition of genetically unrelated and co‐breeding members affects their reproductive success.     

Facultative dispersal by juvenile males in the cooperative stripe-backed wren

We present genetic and demographic data documenting juveniledispersal in the cooperatively breeding stripe-backed wren (Campylorhynchusnuchalis) of Venezuela. Parentage and DNA fragment-sharing analysesrevealed 12 cases in which juveniles were unrelated to othergroup members. Of these 12 foreign juveniles, (1) all were males,(2) eight of 12 had been found with breeding pairs lacking helpersrather than with groups containing helpers, and (3) four outof seven of those observed as adults courted or sired offspringwith the dominant females in their new groups despite the strongincest avoidance of this species. Furthermore, juvenile maleshad a significant tendency to disappear from natal groups intheir first year, and singleton juveniles observed with pairsafter the breeding season were mostly males. These data supportthe hypothesis that foreign juveniles were dispersers from intactgroups and not products of conspecific brood parasitism or adoptionfollowing group dissolution. We suggest that unassisted pairsmight accept juvenile males into their groups as helpers toincrease their future reproductive success and that dispersersthemselves might leave large natal groups in which their helpingis superfluous to join small groups of nonrelatives in whichthey might soon reproduce.     

The relationship between social status, behaviour, growth and steroids in male helpers and breeders of a cooperatively breeding cichlid

We tested whether subordinate helper males of the Lake Tanganyika cooperatively breeding cichlid Neolamprologus pulcher show elevated excretion levels of the stress hormone cortisol and reduced levels of 11-ketotestosterone and testosterone when living in groups with a small breeder male, compared to similar helper males living in groups with a large breeder male, in a full-factorial repeated measures experimental design. We also measured the same hormones in breeder males with and without helper males. Previous research showed that the size difference between large male helpers and male breeders in groups of this species influences behaviour and growth decisions. Contrary to our expectation, no effect of the size-difference between helper males and breeder males on helper hormone levels was detected. Furthermore, helper males had similar hormone excretion levels to those of size-matched breeder males without helpers, and to small breeder males. There was no influence of egg laying on breeder male and helper hormone levels during the experiment. Interestingly, all three hormone levels were significantly lower in helpers showing elevated levels of submissive behaviour towards the breeders, independently of the size of the breeder males. The low cortisol levels suggest that helper males can successfully reduce stress by appeasing breeder males through submission. Furthermore, helper males showing a high level of submissive behaviour had lower levels of androgens than less submissive helpers, suggesting a lower reproductive potential in submissive helpers. We propose that helper submission may be used as an honest signal of reduced interest in reproduction towards the breeder male in this species.     

Experimental evidence for helper effects in a cooperatively breeding cichlid

Neolamprologus pulcher is a cooperatively breeding cichlid fish,in which helpers stay in their natal territory and help withbrood care, territory defense, and maintenance. In this studywe investigated helper effects by an experimental group sizereduction in the field. After this manipulation, focal helpersin reduced groups tended to feed less, and small helpers visitedthe breeding shelter significantly more often than same-sizedhelpers in control groups. No evidence was found that remaininghelpers compensated for the removed helpers by increasing territorydefense and maintenance behavior. Breeders, however, did showa lower defense rate, possibly caused by an increase in broodcare effort. Survival of fry was significantly lower in removalthan control groups, which provides the first experimental proofin a natural population of fish that brood care helpers do effectivelyhelp. The data suggest that in small, generally younger, helpers,kin selection may be an important evolutionary cause of cooperation.Large helpers, however, who are generally older and less relatedto the breeders than small helpers are suggested to pay to beallowed to stay in the territory by helping. All group membersbenefit from group augmentation.     

Cooperative Breeding in the Lake Tanganyika Cichlid Julidochromis ornatus

Cooperative breeding has been described for several cichlids from the genus Julidochromis (Perciformes: Cichlidae) under laboratory conditions, but field evidence is scarce. Here we describe the breeding system of the cichlid Julidochromis ornatus (Boulenger) in Lake Tanganyika (Zambia). Groups defended a breeding shelter under a large flat stone. Smaller group members stayed and fed under or close to the stone, actively guarded by the larger group members. Six out of 28 groups were newly established by breeders, joined by subordinates from a large pool of independent fish (comprising 50–70% of the total population), and four groups were seen to dissolve during a total of 77 observation days. Breeding groups consisted of a large breeding male and female with zero to five smaller subordinates (average 2). Larger breeders and subordinates were found in larger groups. All group members participated in territory defence and -maintenance, but the breeders were only present at the shelter 48% of the time, in contrast to the subordinates which guarded the breeding shelter 94% of the time. Smaller group members showed submissive behaviours to larger group members. We conclude subordinates in J. ornatus are helpers, but we did not find evidence that helpers increased the group’s current reproductive success. Personal observations combined with a literature review revealed at least 19 species of Lake Tanganyika cichlids show evidence of cooperative breeding, entirely confined to the substrate breeding tribe of the Lamprologini (24% of 80 species in total): 2 Chalinochromis spp., 5 Julidochromis spp., 12 Neolamprologus spp. More effort should be put into detecting cooperative breeding in American and Asian substrate breeding cichlid species.     

Size Dependent Male Reproductive Tactic in the Two-Spotted Goby (Gobiusculus flavescens)

Male investment in testes and sperm duct gland in the polygamous nest breeding two-spotted goby Gobiusculus flavescens (Fabricius) was investigated in relation to time in reproductive season and individual physical parameters. This small teleost fish is most likely the most abundant species found along the rocky shores of the North East Atlantic. The two-spotted goby has a single reproductive season, during which nest-caring males can raise several clutches of offspring. According to the literature the males are on average larger than the females. Here we report for the first time a population showing a reversal of this trend, with males on average being smaller than females, a difference likely caused by a large proportion of small males. Early in the breeding season these small males have typical sneaker characters, with relatively large testes and small seminal duct glands compared to the larger dominant territorial males. The presence of these two alternative male reproductive tactics is confirmed by histological studies, which shows the presence of sperm in the sperm duct glands (SDG) of smaller males, but not in the SDG of intermediate and larger males. To our knowledge, males with typical sneaker characters have not been reported in earlier studied populations of two-spotted goby. Interestingly we found that testes investment declined significantly over the course of the breeding season, and that this reduction was significantly more pronounced in small compared to the large males. Further, a significant increase in seminal duct gland (SDG) mass was observed for the smaller males over the breeding season. We propose that this indicates a possible shift in mating tactic by smaller males from a parasitic to a nest-holding tactic over the course of the breeding season. Thus, the observed size dependent plasticity in investment in SDG over time suggests that the reproductive tactic of G. flavescens is conditional, and possibly influenced by mate availability and male—male competition.     

No Evidence for Enforced Alloparental Care in a Cooperatively Breeding Parrot

In cooperatively breeding species, in which non‐breeding helpers assist in rearing the offspring of breeding individuals, conflicts of interest commonly occur between breeders and helpers over their respective contributions to offspring care. During such conflicts, breeders might use aggressive behavior to enforce contributions of helpers to offspring care, especially if helpers are not related to the breeders and their offspring and thus do not stand to gain indirect fitness benefits by helping. Using a combination of behavioral and genetic data, we investigated in the cooperatively breeding El Oro parakeet Pyrrhura orcesi (i) whether breeders are commonly dominant over helpers, (ii) whether they use aggressive behavior toward helpers to enforce offspring provisioning, and (iii) whether the relatedness of helpers to the nestlings affects the frequency of—or the reaction of helpers to—such aggressions. Even though breeders were generally dominant over helpers, we found no evidence for the enforcement of alloparental care. This finding was independent of the relatedness between helpers and nestlings, even though distantly related helpers overall contributed little to offspring care. We suggest that the inability of breeders to properly assess the work rates of their helpers at least partly explains the absence of enforcement. More generally, our results add to a body of evidence suggesting that enforcement might be an exceptional rather than a general mechanism underlying the expression of alloparental care in cooperatively breeding species.